Skip to main content
Log in

Anatomy and ultrastructure of mycorrhizal associations of neotropical Ericaceae

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Ericaceae are obligatory associated with symbiotic fungi forming several, distinctive categories of mycorrhizas. While ericoid, arbutoid, and monotropoid mycorrhizas are known since many years from ericads of the northern hemisphere and the ericoid mycorrhiza also from Australia, a further mycorrhizal category with hyphal sheath, Hartig net, and intracellular colonization was described by us recently and termed cavendishioid mycorrhiza because it was found on Cavendishia nobilis, a species belonging to the Andean clade (Vaccinioideae) of Ericaceae. As the previous findings indicated a correlation between the mycorrhizal category and the systematic position of Ericaceae, we tested the hypothesis that other ericads of the Andean clade might also form cavendishioid mycorrhizas, while ericads occurring in the same area but not belonging to the Andean clade might not. Mycorrhizas of 20 different ericaceous species, 15 belonging to the Andean clade and 5 to other Vaccinioideae or Ericoideae, were sampled in the tropical mountain rain forest area of South Ecuador and investigated by light and electron microscopy. All the 15 members of the Andean clade ericads displayed a hyphal sheath, as well as inter- and intracellular colonization by hyphae as was found on Cavendishia previously. The five species not belonging to the Andean clade ericads displayed only intracellular colonization by hyphae and hence were typical ericoid mycorrhizal. Ultrastructural studies revealed Sebacinales and ascomycetes as mycorrhiza formers in both associations even within one single cell. The results thus support the hypothesis that the Andean clade of Ericaceae forms mycorrhizas distinct from the arbutoid category and most likely presents an independent evolutionary line in the Ericaceae derived from the ericoid mycorrhizas, justifying the new term “cavendishioid mycorrhiza”.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Allen WK, Allaway WG, Cox GC, Valder PG (1989) Ultrastructure of mycorrhizas of Dracophyllum secundum R. Br. Ericales: Epacridaceae. Aust J Plant Physiol 16:147–153

    Google Scholar 

  • Allen TR, Millar T, Berch SM, Berbee ML (2003) Culturing and direct DNA extraction find different fungi from the same ericoid mycorrhizal roots. New Phytol 160:255–272

    Article  CAS  Google Scholar 

  • Bauer R (2004) Basidiomycetous interfungal cellular interaction—a synopsis. In: Agerer R, Blanz P, Piepenbring M (eds) Frontiers in basidiomycote mycology. IHW, Eching, pp 325–337

    Google Scholar 

  • Bauer R, Oberwinkler F (1991) The colacosomes: new structures at the host-parasite interface of a mycoparasitic basidiomycete. Bot Acta 104:53–57

    Google Scholar 

  • Bauer R, Oberwinkler F (2004) 16 Cellular basidiomycete–fungus interactions. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin Heidelberg New York, pp 267–279

    Google Scholar 

  • Beck E, Müller-Hohenstein K (2001) Analysis of undisturbed and disturbed tropical mountain forest ecosystems in Southern Ecuador. Die Erde 132:1–8

    Google Scholar 

  • Berch SM, Allen TR, Berbee ML (2002) Molecular detection, community structure and phylogeny of ericoid mycorrhizal fungi. Plant Soil 244:55–66

    Article  CAS  Google Scholar 

  • Bidartondo MI, Bruns TD (2001) Extreme specificity in epiparasitic Monotropoideae (Ericaceae): widespread phylogenetic and geographical structure. Mol Ecol 10:2285–2295

    Article  PubMed  CAS  Google Scholar 

  • Bonfante-Fasolo P (1980) Occurrence of a basidiomycete in living cells of mycorrhizal hair roots of Calluna vulgaris. Trans Br Mycol Soc 72:320–325

    Google Scholar 

  • Brand F (1991) Ektomykorrhizen an Fagus sylvatica—Charakterisierung und Identifizierung, ökologische Kennzeichnung und unsterile Kultivierung. In: F. Brand (ed) Libri Botanici. IHW, Eching, pp 1–229

    Google Scholar 

  • Brundrett MC (2004) Diversity and classification of mycorrhizal associations. Biol Rev Camb Philos Soc 79:473–495

    Article  PubMed  Google Scholar 

  • Cullings KW (1996) Single phylogenetic origin of ericoid mycorrhizae within the Ericaceae. Can J Bot 74:1896–1909

    CAS  Google Scholar 

  • Gleason FH, McGee PA (2002) Septal pore cap ultrastructure of fungi identified as Epulorhiza sp. (sensu Sebacina) isolated from Australian orchids. Australasian Mycologist 21:12–15

    Google Scholar 

  • Grace C, Stribley DP (1991) A safer procedure for routine staining of vesicular–arbuscular mycorrhizal fungi. Mycol Res 95:1160–1162

    Google Scholar 

  • Harley JL (1969) Biology of myocorrhiza, 2nd edn. Plant Science Monograph, Leonard Hill, London, UK

    Google Scholar 

  • Haug I, Lempe J, Homeier J, Weiss M, Setaro S, Oberwinkler F, Kottke I (2004) Graffenrieda emarginata (Melastomataceae) forms mycorrhizas with Glomeromycota and with a member of the Hymenoscyphus ericae aggregate in the organic soil of a neotropical mountain rain forest. Can J Bot 82:340–356

    Article  Google Scholar 

  • Haug I, Weiss M, Homeier F, Oberwinkler F, Kottke I (2005) Russulaceae and Telephoraceae form ectomycorrhizas with members of the Nyctaginaceae (Caryophyllales) in the tropical mountain rain forest of southern Ecuador. New Phytol 165:923–936

    Article  PubMed  CAS  Google Scholar 

  • Homeier J (2004) Baumdiversität, Waldstruktur und Wachstumsdynamik zweier tropischer Bergregenwälder in Ecuador und Costa Rica. Ph.D. thesis, University of Bielefeld, Bielefeld, Germany

  • Kottke I, Oberwinkler F (1988) Comparative studies on the mycorrhization of Larix decidua and Picea abies by Suillus grevillei. Trees 2:115–128

    Article  Google Scholar 

  • Kreger-van Rij NJB, Veenhuis M (1971) A comparative study of the cell wall structure of basidiomycetous and related yeasts. J Gen Microbiol 68:87–95

    Google Scholar 

  • Kron KA, Luteyn JL (2005) Origins and biogeographic patterns in Ericaceae: new insights from recent phylogenetic analyses. Biol Skr 55:479–500

    Google Scholar 

  • Kron KA, Judd WS, Stevens PF, Crayn DM, Anderberg AA, Gadek PA, Quinn CJ, Luteyn JL (2002) Phylogenetic classification of Ericaceae: molecular and morphological evidence. Bot Rev 68:335–423

    Article  Google Scholar 

  • Luteyn JL (1989) Speciation and diversity of Ericaceae in Neotropical montane vegetation. In: Holm-Nielsen LB, Nielsen IC, Balslev H (eds) Tropical forests, botanical dynamics, speciation and diversity. Academic, London, pp 297–310

    Google Scholar 

  • Luteyn J (1996) 147. Ericaceae. In: Harling G, Andersson L (ed) Flora of Ecuador. Department of Systematic Botany, University of Göteborg, Stockholm, Sweden, pp 1–404

  • Luteyn JL (2002) Diversity, adaptation, and endemism in neotropical Ericaceae: biogeographical patterns in the Vaccinieae. Bot Rev 68:55–87

    Article  Google Scholar 

  • Massicotte HB, Melville LH, Peterson RL (2005) Structural characteristics of root–fungal interactions for five ericaceous species in eastern Canada. Can J Bot 83:1057–1064

    Article  Google Scholar 

  • Molina R, Trappe JM (1982) Lack of mycorrhizal specificity by ericaceous hosts Arbutus menziesii and Arctostaphylos uva-ursi. New Phytol 90:495–509

    Article  Google Scholar 

  • Münzenberger B, Kottke I, Oberwinkler F (1992) Ultrastructural investigations of Arbutus unedo–Laccaria amethystea mycorrhiza synthesized in vitro. Trees 7:40–47

    Article  Google Scholar 

  • Perotto S, Girlanda M, Martino E (2002) Ericoid mycorrhizal fungi: some new perspectives on old acquaintances. Plant Soil 244:41–53

    Article  CAS  Google Scholar 

  • Peterson TA, Mueller WC, Englander L (1980) Anatomy and ultrastructure of a Rhododendron root–fungus association. Can J Bot 58:2421–2433

    Google Scholar 

  • Powell EA, Kron KA (2003) Molecular systematics of the northern Andean blueberries (Vaccinieae, Vaccinioideae, Ericaceae). Int J Plant Sci 164:987–995

    Article  CAS  Google Scholar 

  • Rains KC, Nadkarni NM, Bledsoe CS (2003) Epiphytic and terrestrial mycorrhizas in a lower mountain Costa Rican cloud forest. Mycorrhiza 13:257–264

    Article  PubMed  Google Scholar 

  • Richter M (2003) Using epiphytes and soil temperatures for eco-climatic interpretations in southern Ecuador. Erdkunde 57:161–181

    Google Scholar 

  • Robertson DC, Robertson JA (1985) Ultrastructural aspects of Pyrola mycorrhizae. Can J Bot 63:1089–1098

    Google Scholar 

  • Schüssler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Google Scholar 

  • Selosse M-A, Bauer R, Moyersoen B (2002) Basal hymenomycetes belonging to the Sebacinaceae are ectomycorrhizal on temperate deciduous trees. New Phytol 155:183–195

    Article  CAS  Google Scholar 

  • Setaro S, Weiss M, Oberwinkler F, Kottke I (2006) Sebacinales form ectendomycorrhizas with Cavendishia nobilis, a member of the Andean clade of Ericaceae, in the mountain rain forest of southern Ecuador. New Phytol 169:355–365

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, London, UK

    Google Scholar 

  • Soethe N, Lehmann J, Engels C (2006) Root morphology and anchorage of six native tree species from a tropical montane forest and an elfin forest in Ecuador. Plant Soil 279:173–185

    Article  CAS  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Turnau K, Kottke I, Oberwinkler F (1993) Comparative study of elongated and globose Woronin bodies using electron energy loss spectroscopy (EELS) and imaging (ESI). Mycol Res 97:1499–1504

    Article  Google Scholar 

  • Urban A, Weiss M, Bauer R (2003) Ectomycorrhizas involving sebacinoid mycobionts. Mycol Res 107:3–14

    Article  PubMed  Google Scholar 

  • Vrålstad T, Fossheim T, Schumacher T (2000) Piceirhiza bicolorata—the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytol 145:549–563

    Article  Google Scholar 

  • Vrålstad T, Schumacher T, Taylor AF (2002) Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytol 153:143–152

    Article  Google Scholar 

  • Weiss M, Oberwinkler F (2001) Phylogenetic relationships in Auriculariales and related groups—hypotheses derived from nuclear ribosomal DNA sequences. Mycol Res 105:403–415

    Article  CAS  Google Scholar 

  • Weiss M, Selosse M-A, Rexer K-H, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010

    Article  PubMed  Google Scholar 

  • Wilcke W, Yasin S, Abramowsky U, Valarezo C, Zech W (2002) Nutrient storage and turnover in organic layers under tropical mountain rain forest in Ecuador. Eur J Soil Sci 53:15–27

    Article  CAS  Google Scholar 

  • Williams PG, Thilo E (1989) Ultrastructural evidence for the identity of some multinucleate rhizoctonias. New Phytol 112:513–518

    Article  Google Scholar 

  • Zak B (1974) Ectendomycorrhiza of Pacific Madrone (Arbutus menziesii). Trans Br Mycol Soc 62:202–204

    Article  Google Scholar 

  • Zak B (1976) Pure culture synthesis of Pacific Madrone ectendomycorrhizae. Mycologia 68:362–369

    Google Scholar 

Download references

Acknowledgments

We thank James L. Luteyn and Paola Pedraza for the identification of the plant material. We are grateful to Ingeborg Haug for critically reading earlier drafts of the manuscript. The study was carried out within the DFG research project FOR 402-2, whose financial support is highly appreciated. We thank the NCI for providing research facilities.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sabrina Setaro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Setaro, S., Kottke, I. & Oberwinkler, F. Anatomy and ultrastructure of mycorrhizal associations of neotropical Ericaceae. Mycol Progress 5, 243–254 (2006). https://doi.org/10.1007/s11557-006-0516-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-006-0516-7

Keywords

Navigation